Organizational requirements for multicellular autonomy: insights from a comparative case study

In this paper we explore the organizational conditions underlying the emergence of organisms at the multicellular level. More specifically, we shall propose a general theoretical scheme according to which a multicellular organism is an ensemble of cells that effectively regulates its own development through collective (meta-cellular) mechanisms of control of cell differentiation and cell division processes. This theoretical result derives from the detailed study of the ontogenetic development of three multicellular systems (Nostoc punctiforme, Volvox carteri and Strongylocentrotus purpuratus) and, in particular, of their corresponding cell-to-cell signaling networks. The case study supports our claim that a specific type of functional integration among the cells of a multicellular ensemble (namely, a regulatory control system consisting in several inter-cellular mechanisms that modulate epigenesis and whose operation gets decoupled from the intra-cellular metabolic machinery), is required for it to qualify as a proper organism. Finally, we argue why a multicellular system exhibiting this type of functionally differentiated and integrated developmental organization becomes a self-determining collective entity and, therefore, should be considered as a second-order autonomous system.